Biotechnology & Biotechnological Equipment

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Biosorption of Pb(II) ions from aqueous solutions

by waste biomass of Streptomyces fradiae
pretreated with NaOH

Gergana Kirova, Zdravka Velkova, Margarita Stoytcheva, Yana Hristova, Ivan

Iliev & Velizar Gochev

To cite this article: Gergana Kirova, Zdravka Velkova, Margarita Stoytcheva, Yana Hristova,
Ivan Iliev & Velizar Gochev (2015) Biosorption of Pb(II) ions from aqueous solutions by waste
biomass of Streptomyces fradiae pretreated with NaOH, Biotechnology & Biotechnological
Equipment, 29:4, 689-695, DOI: 10.1080/13102818.2015.1036775

To link to this article: http://dx.doi.org/10.1080/13102818.2015.1036775

2015 The Author(s). Published by Taylor &

Francis.

Published online: 27 Apr 2015.

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 Biotechnology & Biotechnological Equipment, 2015
Vol. 29, No. 4, 689
695, http://dx.doi.org/10.1080/13102818.2015.1036775

ARTICLE; AGRICULTURE AND ENVIRONMENTAL BIOTECHNOLOGY

Biosorption of Pb(II) ions from aqueous solutions by waste biomass of Streptomyces fradiae
pretreated with NaOH
Gergana Kirovaa, Zdravka Velkovaa, Margarita Stoytchevab, Yana Hristovac, Ivan Ilievc and Velizar Gochevc*
a
Faculty of Pharmacy, Department of Chemistry and Biochemistry, Medical University of Plovdiv, Plovdiv, Bulgaria; bInstituto de
Ingenier
a, Autonomous University of Baja California, Baja California, Mexicali, Mexico; cFaculty of Biology, Department of
Biochemistry and Microbiology, University of Plovdiv Paisii Hilendarski, Plovdiv, Bulgaria

(Received 27 February 2015; accepted 30 March 2015)

Biosorption of Pb(II) ions from a model solution was investigated using Streptomyces fradiae biomass as biosorbent
pretreated with sodium hydroxide. The mycelium is a waste product from the biotechnological production of the macrolide
antibiotic tylosin in the pharmaceutical industry. The biosorption study was conducted in a batch system with respect to
initial pH, initial metal concentration and contact time. For a description of the biosorption equilibrium, Langmuir and
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Freundlich adsorption models were used. Equilibrium data fitted better to the Langmuir model and the calculated
maximum biosorption capacity was 138.88 mgg1 at initial pH 5.0, contact time of 120 min, biosorbent dose of 1 gdm3
and concentration range for the Pb(II) ions from 10 to 200 mgdm3. Pseudo-first and pseudo-second order kinetic models
were applied to the experimental data. The results indicated that the Pb(II) uptake process followed the Ho equation. The
interference of co-present ions Cu(II) and Zn(II) on the Pb(II) biosorption was also studied. It was determined that at the
highest Pb(II) concentration (200 mgdm3) Cu(II) and Zn(II) caused 27.22% and 24.88% decreasing in Pb(II) uptake,
respectively. The obtained results could be useful in prospective applications of chemically modified waste mycelium of S.
fradiae as an alternative biosorbent for Pb(II) removal from aqueous solutions.
Keywords: biosorption; toxic metals; Streptomyces; isotherm; kinetics

Introduction cells: no requirement for growth media and nutrients; low

Environmental pollution caused by heavy metals present
in different effluents is a serious public health problem,
due to their toxicity even in very low concentrations. The
problem concerns mainly aquatic ecosystems, where toxic
metals could concentrate in food chains even at very low
levels of water contamination.
Various methods have been proposed for removal of
metal ions from aqueous solutions, such as hydroxide or
sulfide precipitation, ion exchange, reverse osmosis, evap-
oration, electrodeposition.[1] These methods are not
completely satisfactory because of their relatively high
costs and/or production of large volumes of sludge that
must be treated or eliminated, resulting in surplus costs.
Among the biological methods, bioaccumulation and
biosorption demonstrate promising potential for replacing
conventional methods for metal concentration and
removal from aqueous solutions. Bioaccumulation is a
process that occurs only in living organisms through
transport of contaminants and their accumulation into the
cell.[2] In the biosorption process, metal ions are adsorbed
on the surface of dead biomass as a sorbent. Thus, bio-
sorption is a metabolically passive process. The use of
dead biomass offers the following advantages over living
cost; high efficiency; minimization of chemical sludge;
regeneration of biosorbent and possibility for metal
recovery.[3]
Various microorganisms, such as bacteria, yeast and
fungi, have been studied for Pb(II) removal from aqueous
solutions.[3
10] Waste microbial mycelium from antibi-
otic-producing Streptomyces species is a major by-product
of the biopharmaceutical industry and its disposal causes
serious ecological problems. Such biomasses were studied
for Cd(II),[11,12] Cr(III),[13] Pb(II) [14] and Ni(II) [15]
biosorption.
To the best of our knowledge, only Simeonova et al.
[16] and Kirova et al. [17] have studied the possibilities
for application of dead mycelium of tylosin-producing
Streptomyces fradiae for Cu(II), Zn(II) and Ni(II) removal
from aqueous solutions.
The goal of the present work was to investigate the
biosorption potential of S. fradiae waste biomass pre-
treated with sodium hydroxide for removal of Pb(II) ions
from aqueous solution. The effects of pH, contact time
and initial metal concentration on the biosorption capacity
of the biomass were studied. The biosorption of Pb(II)
was characterized by the Langmuir and Freundlich

*Corresponding author. Email: vgochev@uni-plovdiv.bg

2015 The Author(s). Published by Taylor & Francis.

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unre-
stricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
 690 G. Kirova et al.
models. The kinetics of biosorption of Pb(II) ions was
described using pseudo-first order and pseudo-second
order models. The interference of co-present ions, copper
and zinc, on the Pb(II) biosorption capacity was also
studied.
Materials and methods
Biosorbent preparation
Waste Streptomyces fradiae biomass was provided by
Biovet AD, Peshtera, Bulgaria. The raw biomass was
powdered by mortar and pestle, filtered under vacuum,
washed several times with distilled water until pH 6 was
reached in the filtrate and oven-dried at 80  C for 12 h.
The dried biomass was stored at 4  C until further use.
Five grams of the heat inactivated biomass were boiled at
110  C for 15 min in 100 cm3 of 1 moldm3 NaOH. The
alkali-treated biomass was filtered under vacuum, washed
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with distilled water and oven-dried at 80  C for 12 h. The
dried biomass was stored at 4  C until further use.
Model solutions
3
Pb(II) stock solution (1000 mgdm ) was prepared from
analytical grade Pb(NO3)2 (Merck, Darmstadt, Germany)
in deionized water containing 10 cm3 concentrated nitric
acid. Working solutions were prepared immediately
before use by adequate dilution.
Fourier transform infrared spectroscopy (FTIR)
analysis
The functional groups present on the surface of the pre-
treated S. fradiae biomass before and after Pb(II) sorption
were determined by FTIR analysis, using a Thermo Nico-
let Avatar 330 FT-IR spectrometer (Thermo Electronic
Corporation). The samples were prepared as KBr discs
and the FTIR spectra were recorded in the region of
4000
400 cm1.
Biosorption of Pb(II) from single solutions
In order to evaluate the effect of pH, initial Pb(II) concen-
tration and contact time, a set of biosorbtion experiments
were carried out in a batch system. The pH of metal solu-
tions was adjusted to values between 2.0 and 5.0, using
0.1 moldm3 HNO3 or 0.1 moldm3 NaOH. Biosorption
of Pb(II) was carried out in 250 cm3 Erlenmeyer flasks by
adding 0.1 g of biosorbent to 100 cm3 metal solution of a
desired concentration and pH value at 25 1  C, on a
magnetic stirrer with a speed of 300 rmin1 for 120 min.
Samples were taken at definite time intervals and centri-
fuged at 3000 rmin1 for 10 min. The concentration of
Pb(II) ions in the liquid supernatant was determined.
Biosorption of Pb(II) ions from binary model solutions
To determine the biosorption characteristics of Pb(II) ions
in binary metal solutions, the initial concentration of
Pb(II) ions was varied between 10 and 200 mgdm3,
whereas the concentrations of Cu(II) or Zn(II) ions were
25 mgdm3. The experiments were carried out at optimal
pH value for Pb(II) biosorption, as determined for the sin-
gle metal-ion solution, and using the same procedures as
in the single biosorption experiments.
All glassware used in the biosorption experiments was
washed with 10% HNO3 and subsequently rinsed with
deionized water to avoid binding of the metal ions to it.
Analysis of metal ions
The residual metal concentrations in the supernatants
were determined using a Perkin Elmer atomic absorption
spectrometer PinAAcle 900 T (THGA/FLAME) at
283.31 nm.
Calculation of metal uptake and removal efficiency
The metal uptake was calculated by the simple difference
method [18]:
q D Ci Cf V =W ; (1)
The removal of metal ions was determined using
Equation (2):
R D Ci Cf =Ci 100; % (2)
where Ci and Cf are the initial and final concentration of
Pb(II) in solution (mgdm3); V is the volume of the
solution in the flask (dm3); and W is the mass of the bio-
sorbent (g).
Equilibrium modelling
The Langmuir and Freundlich models were used to
describe the biosorption equilibrium [19]. The linearized
Langmuir isotherm allows the calculation of the maxi-
mum adsorption capacity and Langmuir constant and was
presented by the following equation:
Ce =qe D 1=qm Ce C 1=bqm (3)
where qe and qm are the metal uptake at equilibrium and
the maximum metal uptake, respectively, (mgg1); Ce is
the metal concentration at equilibrium (mgdm3) and b
is the constant related to the affinity of the binding sites
(dm3mg1).

The Freundlich isotherm was linearized as follows and
Freundlich constants were determined:
lgqe D lg KF C 1=n lgCe (4)
where KF (dm3g1) and n (dimensionless) are the Freund-
lich adsorbent constant and the exponent characterizing
the system.
Kinetic models
In order to evaluate the biosorption processes of Pb(II)
ions on NaOH-pretreated S.fradiae biomass, pseudo-first
and pseudo-second order kinetic models were used.
After integration and applying boundary conditions
t D 0 to t D t and qt D 0 to qt D qt, the pseudo-first order
equation was given as [20]:
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lg qe qt D lgqe k1 =2:303t (5) mass showed presence of hydroxyl, carboxyl and amine
where qt and qe are the biosorption uptake of Pb(II) ions at
time t and at equilibrium (mgg1); k1 is the pseudo-first
order rate constant (min1) and t is the contact time (min).
By plotting lg(qe qt) against t, the values of qe and
k1 can be calculated by the intercept and the slope of the
plot, respectively.
The pseudo-second order rate equation [21] was
expressed in a linear form as:
t=qt D 1=k2 q2e C 1=qe t (6)
where k2 is the pseudo-second order rate constant
(gmg1min1). most critical parameters influencing the biosorption pro-
The plot of (t/qt) and t of this equation give a linear
relationship from which qe and k2 were determined.
Results and discussion
FTIR analysis
Biosorption is defined as the property of microorganisms
to accumulate metal ions by adsorption on the cell sur-
face. The major constituent of the Streptomyces cell wall
is peptidoglycan linked with teichoic acid and polysac-
charides. The functional groups of these molecules can
play an important role in the biosorption of metal ions.
[22
24] For this reason, to study the mechanism of Pb(II)
removal by waste NaOH-treated S. fradiae mycelium
from tylosin production, the active chemical groups on
the cell surface before and after Pb(II) removal were eval-
uated by FTIR spectroscopy. The obtained results are
shown in Figure 1.
The spectrum of the waste S. fradiae biomass treated
with NaOH showed several bands. The broad and strong
band at 3415.48 cm1 could be attributed to the
Biotechnology & Biotechnological Equipment 691
overlapping of
OH and
NH stretching. The presence
of
CH stretching vibrations was confirmed by the
adsorption peaks at 2921.48 and 2850.41 cm1. The
stretching of
OH groups could occur from carboxylic
acids and the peak is extremely broad in the range from
3400 to 2400 cm1 and often interferes with the adsorp-
tion of
CH groups.[23] The bands at 1652.84 and
1562.14 cm1 could be assigned to amide I (
C
O
stretching coupled with
N
H deformation mode) and
amide II (
N
H deformation coupled to
C D N

deformation) and/or asymmetric stretching vibration of
COO groups, respectively. The peak at 1461.85 cm1
corresponds to bending deformations of
CH2 or
OH
bending in carboxylic groups. The peaks situated at
1411.70 cm1 and 1041.42 cm1 could be due to symmet-
ric stretching of COO vibrational stretching and/or
stretching of ?
= of alcohols and C
?
E groups. Thus,
the FTIR analysis of the pretreated waste S. fradiae bio-
groups on the biosorbent surface.
The FTIR spectra of the metal loaded biomass, which
is presented in Figure 1(b), showed that the peaks
expected at 3415.48, 1652.84, 1562.14, 1461.85, 1411.71
and 1041.42 cm1 were changed and shifted to 3363.41,
1658.56, 1540.92, 1456.06, 1415.56 and 1031.78 cm1.
The cause of these shifts is difficult to be determined, but
the results revealed interactions between the Pb(II) ions,
hydroxyl, amino and carboxyl groups on the biomass sur-
face similar to those reported by other authors [8,13,23].
Effect of pH
The pH of the aqueous solution is considered as one of the
cesses. It affects the behaviour and speciation of metal
ions; the dissociation of functional groups on the active
sites of the biosorbent and the metal ion
sorbent interac-
tions.[25] To avoid precipitation of metal hydroxides, the
initial pH of the solution was chosen according to the spe-
ciation diagram for Pb(II) ions. The dominant species in
the pH range from 2.0 to 5.0 were Pb2C and Pb(OH)C and
at pH values higher than 5, several low-soluble hydroxide
species are observed.[26]
The effect of the initial pH on the Pb(II) removal by
waste NaOH-pretreated S. fradiae biomass was evaluated
in the range from 2.0 to 5.0 to avoid Pb(OH)2 precipita-
tion. The results are shown in Figure 2.
The biosorption efficiency increased from 75.2% to
97.68% with the increase in pH from 2.0 to 5.0. The high-
est metal uptake (48.84 mgg1) was obtained at pH 5.0.
Therefore, pH 5.0 was selected for all further experiments.
These results could be explained by the fact that as pH
increases, this causes deprotonation of functional groups
on the cell wall of the biosorbent. Thus, negatively
charged sites are formed and they electrostatically attract
 692 G. Kirova et al.
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Figure 1 . FTIR spectra of the waste S. fradiae biomass before (a) and after (b) Pb(II) biosorption.
positively charged metal ions. The low removal efficiency
at low pH was apparently due to the presence of higher
concentrations of hydrogen ions in the solution which
Figure 2. Effect of pH on biosorption of Pb(II) by waste
S. fradiae biomass. Note: Ci D 50 mgdm3, V D 100 cm3,
W D 1 gdm3, t D 120 min.
competed with Pb(II) ions for the adsorption sites on the
biosorbent surface. These results were in good agreement
with data for the effect of pH on Pb(II) biosorption
reported by other authors.[7,8,13,25]
Effect of contact time and initial concentration of Pb(II)
on biosorption uptake
The effect of contact time on the biosorption uptake of
Pb(II) ions using NaOH-pretreated S. fradiae biomass at
different initial concentrations is illustrated in Figure 3.
As shown, at an initial Pb(II) concentration of
25 mgdm3, the Pb(II) uptake was rapid and equilib-
rium was reached within the first 20 min. For 50 and
100 mgdm3, equilibrium was reached after 30 and
80 min, respectively. After 120 min, the Pb(II) uptake
was 24.70 48.84 and 89.23 mgg1 when 25, 50 and
100 mgdm3 initial Pb(II) concentrations were used.
Thus, 120 min were selected as an optimum contact
time for further experiments. These results are in agree-
ment with the reports of Selatnia et al. [14] and Simeo-
nova et al. [16].

Figure 3. Effect of contact time and initial Pb(II) concentration
on the NaOH-pretreated S. fradiae biomass biosorption capacity.
Note: pH D 5.0, V D 100 cm3, W D 1 gdm3, t D 120 min, Ci D
25, 50, 100 mgdm3.
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Adsorption isotherm analysis
Proper quantification of the sorption equilibrium is
required for commercial-scale application of the biosorp-
tion technique. The Langmuir and Freundlich isotherms
are more frequently used. The Langmuir adsorption iso-
therm is based on the assumption that the surface is homo-
geneous, with all the adsorption sites having equal
adsorbate affinity and adsorption at one site not affecting
the adsorption at an adjacent site. The Freundlich adsorp-
tion isotherm describes heterogeneous surface adsorption
and does not assume monolayer biosorption.[22] The line-
arized forms of the Langmuir and Freundlich isotherms
are presented in Figures 4 and 5, respectively.
The calculated model constants and correlation coeffi-
cients for Pb(II) biosorption by NaOH-treated S. fradiae
biomass are given in Table 1.
Figure 4. Linear plot of the Langmuir isotherm.
Biotechnology & Biotechnological Equipment 693
Figure 5. Linear plot of the Freundlich isotherm.
The experimental data fitted better to the Langmuir
model compared to the Freundlich model. The maximum
Pb(II) uptake per unit of dry S. fradiae biomass treated
with NaOH was found to be 138.88 mgg1. These results
are comparable with the maximum biosoprtion capacity
of NaOH-treated dead biomass of Streptomyces rimosus
(135 mgg1) obtained by Selatnia et al. [14]. The authors
carried out the Pb(II) removal from aqueous solutions at
contact time of 3 h, biomass concentration of 3 gdm3
and a stirring speed of 250 rmin1. However, it is note-
worthy that the maximum biosorption capacity is a func-
tion of the experimental conditions. That is why it is
generally very difficult to compare the results from a par-
ticular experiment with those in other reports where bio-
sorption experiments have been performed at different
process parameters.
Kinetic studies
Various kinetic models could be used for analysis of the
biosorption process. In the present study, pseudo-first and
pseudo-second order models were applied to the kinetic
experimental data (Figures 6 and 7). The calculated
Lagergren and Ho kinetic constants for biosorption of
Pb(II) by waste S. fradiae biomass and their correspond-
ing regression correlation coefficients are presented in
Table 2.
The correlation coefficients for the pseudo-second
order model were very high for all the Pb(II)
Table 1. Isotherm model constants and correlation coefficients
for biosorption of Pb(II) ions.
Langmuir model Freundlich model
qm, mgg1 b, dm3mg1 R2 KF, dm3g1 n R2
138.88 0.360 0.997 35.31 2.61 0.964
 694 G. Kirova et al.

Figure 6. Linear plot of pseudo-first kinetic model. Note: Ci D

25, 50, 100 mgdm3.
Figure 8. Biosorption of Pb(II) onto S. fradiae biomass. Notes:
1
Pb(II) ions only; 2
Pb(II) and Cu(II) ions; 3
Pb(II) and
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Zn(II) ions.

view it is very important to clarify the influence of co-

Figure 7. Linear plot of pseudo-second kinetic model. Note: Ci
D 25, 50, 100 mgdm3.
concentrations studied by us. The calculated equilibrium
uptakes for the Pb(II) ions indicated that this model fitted
better to the experimental values.
present ions, such as Cu(II) and Zn(II), onto Pb(II)
removal from aqueous solutions by NaOH pretreated
waste mycelium of S. fradiae. The obtained results are
shown in Figure 8.
It was obtained that the co-present ions decreased the
effectiveness of waste biomass of S. fradiae as a Pb(II)
biosorbent. When the initial Pb(II) concentration was
200 mgdm3, the presence of Cu(II) ions caused a
27.22% decrease in the biosorption uptake of Pb(II). The
decrease was similar in the presence of Zn(II) ions
(24.88%). This similarity in the effect of Zn(II) and Cu(II)
on the Pb(II) biosorption could be explained by the simi-
larity between copper and zinc in terms of molecular mass
(63.57 and 65.38), ionic radii (73 and 74 pm) and electro-
negativity (1.90 and 1.65 Pauling) and their covalent indi-
ces (xm2r), which are 6.41 and 4.54, respectively [9].

Effect of interfering ions on Pb(II) biosorption Conclusions

Available studies report mostly biosorption experiments The biosorption capacity of NaOH pretreated S. fradiae
carried out in single-ion model solutions; however, indus- biomass, a waste product from the industrial biotechno-
trial wastewaters are usually polluted with more than one logical production of the macrolide antibiotic tylosin, was
heavy metal. For this reason, from a practical point of studied for Pb(II) ions removal from dilute aqueous

Table 2. Kinetic constants for Pb(II) biosorption by waste S. fradiae biomass.

Pseudo-first order kinetic model Pseudo-second order kinetic model

Pb(II) initial concentration, mgdm3 qe, mgg1 k1, min1 R2 qe, mgg1 k2, gmg1min1 R2

25 10.08 10.7 102 0.995 25.86 19.7 103 0.999

50 27.65 8.8 102 0.971 54.74 3.7 103 0.996
100 55.19 5.6 102 0.993 91.82 2.0 103 0.997

solutions. The optimal process parameters were initial pH
5.0 and contact time 120 min. The experimental data at the
studied conditions fitted well to the Langmuir adsorption
isotherm and maximum Pb(II) uptake of 138.88 mg g1
was calculated. The kinetic of Pb(II) biosorption onto
chemically modified waste biomass of S. fradiae followed
a pseudo-second order model. The obtained results suggest
that chemically modified waste mycelium of S. fradiae
could be considered a prospective and cheap alternative
biosorbent for Pb(II) removal from aqueous solutions but
can show decreased effectiveness caused by co-present
ions. Further experiments will be focused on the optimiza-
tion of process parameters for Pb(II) desorption and
recovery of the biosorbent for reusage. The obtained
results are a basis for development of environmentally
friendly biotechnology for purification of wastewaters con-
taminated with heavy metals through utilization of waste
mycelium from antibiotic production.
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Disclosure statement
No potential conflict of interest was reported by the authors.
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